Modeling Structural Dynamics of Biomolecular Complexes by Coarse-Grained Molecular Simulations

Accounts of Chemical Research

Volumn 48, Issue 12, 2015, Pages 3026-3035

  Takada, Shoji ^a   Kanada, Ryo ^a   Tan, Cheng ^a   Terakawa, Tsuyoshi ^b   Li, Wenfei ^c   Kenzaki, Hiroo ^d  

^a KYOTO UNIVERSITY   (Japan)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c NANJING UNIVERSITY   (China)

^d RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PROTEIN;

CHEMISTRY; MOLECULAR DYNAMICS;

DNA; MOLECULAR DYNAMICS SIMULATION; PROTEINS;

EID: 84949816970     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/acs.accounts.5b00338     Document Type: Article

References (58)

1. The Nobel Prize in Chemistry 2013, Advanced Information Nobelprize.org.
2. Kenzaki, H.; Koga, N.; Hori, N.; Kanada, R.; Li, W.; Okazaki, K. I.; Yao, X. Q.; Takada, S. CafeMol: A Coarse-Grained Biomolecular Simulator for Simulating Proteins at Work J. Chem. Theory Comput. 2011, 7 (6) 1979-1989 10.1021/ct2001045
3. Tozzini, V. Multiscale Modeling of Proteins Acc. Chem. Res. 2010, 43 (2) 220-230 10.1021/ar9001476
4. Hyeon, C.; Thirumalai, D. Capturing the Essence of Folding and Functions of Biomolecules Using Coarse-Grained Models Nat. Commun. 2011, 2, 487 10.1038/ncomms1481
5. Ingólfsson, H. I.; Lopez, C. A.; Uusitalo, J. J.; de Jong, D. H.; Gopal, S. M.; Periole, X.; Marrink, S. J. The Power of Coarse Graining in Biomolecular Simulations Wiley Interdiscip. Rev. Comput. Mol. Sci. 2014, 4 (3) 225-248 10.1002/wcms.1169
6. Doye, J. P. K.; Ouldridge, T. E.; Louis, A. A.; Romano, F.; Sulc, P.; Matek, C.; Snodin, B. E. K.; Rovigatti, L.; Schreck, J. S.; Harrison, R. M.; Smith, W. P. J. Coarse-Graining DNA for Simulations of DNA Nanotechnology Phys. Chem. Chem. Phys. 2013, 15 (47) 20395-20414 10.1039/c3cp53545b
7. Liwo, A.; He, Y.; Scheraga, H. A. Coarse-Grained Force Field: General Folding Theory Phys. Chem. Chem. Phys. 2011, 13 (38) 16890-16901 10.1039/c1cp20752k
8. Ozer, G.; Luque, A.; Schlick, T. The Chromatin Fiber: Multiscale Problems and Approaches Curr. Opin. Struct. Biol. 2015, 31, 124-139 10.1016/j.sbi.2015.04.002
9. Davtyan, A.; Schafer, N. P.; Zheng, W.; Clementi, C.; Wolynes, P. G.; Papoian, G. A. AWSEM-MD: Protein Structure Prediction Using Coarse-Grained Physical Potentials and Bioinformatically Based Local Structure Biasing J. Phys. Chem. B 2012, 116 (29) 8494-8503 10.1021/jp212541y
10. Takada, S. Coarse-Grained Molecular Simulations of Large Biomolecules Curr. Opin. Struct. Biol. 2012, 22 (2) 130-137 10.1016/j.sbi.2012.01.010
11. Bryngelson, J. D.; Wolynes, P. G. Spin Glasses and the Statistical Mechanics of Protein Folding Proc. Natl. Acad. Sci. U. S. A. 1987, 84 (21) 7524-7528 10.1073/pnas.84.21.7524
12. Bryngelson, J. D.; Onuchic, J. N.; Socci, N. D.; Wolynes, P. G. Funnels, Pathways, and the Energy Landscape of Protein Folding: A Synthesis Proteins: Struct., Funct., Genet. 1995, 21 (3) 167-195 10.1002/prot.340210302
13. Leopold, P. E.; Montal, M.; Onuchic, J. N. Protein Folding Funnels: A Kinetic Approach to the Sequence-Structure Relationship Proc. Natl. Acad. Sci. U. S. A. 1992, 89 (18) 8721-8725 10.1073/pnas.89.18.8721
14. Clementi, C. Coarse-Grained Models of Protein Folding: Toy Models or Predictive Tools? Curr. Opin. Struct. Biol. 2008, 18, 10-15 10.1016/j.sbi.2007.10.005
15. Tirion, M. M. Large Amplitude Elastic Motions in Proteins from a Single-Parameter, Atomic Analysis Phys. Rev. Lett. 1996, 77, 1905-1908 10.1103/PhysRevLett.77.1905
16. Tama, F.; Valle, M.; Frank, J.; Brooks, C. L. Dynamic Reorganization of the Functionally Active Ribosome Explored by Normal Mode Analysis and Cryo-Electron Microscopy Proc. Natl. Acad. Sci. U. S. A. 2003, 100 (16) 9319-9323 10.1073/pnas.1632476100
17. Wang, Y.; Rader, A. J.; Bahar, I.; Jernigan, R. L. Global Ribosome Motions Revealed with Elastic Network Model J. Struct. Biol. 2004, 147 (3) 302-314 10.1016/j.jsb.2004.01.005
18. Ikeguchi, M.; Ueno, J.; Sato, M.; Kidera, A. Protein Structural Change upon Ligand Binding: Linear Response Theory Phys. Rev. Lett. 2005, 94 (7) 078102 10.1103/PhysRevLett.94.078102
19. Bahar, I.; Lezon, T. R.; Yang, L.-W.; Eyal, E. Global Dynamics of Proteins: Bridging between Structure and Function Annu. Rev. Biophys. 2010, 39, 23-42 10.1146/annurev.biophys.093008.131258
20. Go, N. Theoretical Studies of Protein Folding Annu. Rev. Biophys. Bioeng. 1983, 12, 183-210 10.1146/annurev.bb.12.060183.001151
21. Takada, S. Go-Ing for the Prediction of Protein Folding Mechanisms Proc. Natl. Acad. Sci. U. S. A. 1999, 96 (21) 11698-11700 10.1073/pnas.96.21.11698
22. Clementi, C.; Nymeyer, H.; Onuchic, J. N. Topological and Energetic Factors: What Determines the Structural Details of the Transition State Ensemble and "En-Route" Intermediates for Protein Folding? An Investigation for Small Globular Proteins J. Mol. Biol. 2000, 298 (5) 937-953 10.1006/jmbi.2000.3693
23. Koga, N.; Takada, S. Roles of Native Topology and Chain-Length Scaling in Protein Folding: A Simulation Study with a Go-like Model J. Mol. Biol. 2001, 313 (1) 171-180 10.1006/jmbi.2001.5037
24. Karanicolas, J.; Brooks, C. L. Improved G??-like Models Demonstrate the Robustness of Protein Folding Mechanisms towards Non-Native Interactions J. Mol. Biol. 2003, 334 (2) 309-325 10.1016/j.jmb.2003.09.047
25. Koga, N.; Takada, S. Folding-Based Molecular Simulations Reveal Mechanisms of the Rotary Motor F1-ATPase Proc. Natl. Acad. Sci. U. S. A. 2006, 103 (14) 5367-5372 10.1073/pnas.0509642103
26. Hoang, T. X.; Cieplak, M. Sequencing of Folding Events in Go-Type Proteins J. Chem. Phys. 2000, 113 (18) 8319-8328 10.1063/1.1314868
27. Hyeon, C.; Thirumalai, D. Mechanical Unfolding of RNA Hairpins Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 6789-6794 10.1073/pnas.0408314102
28. Noel, J. K.; Whitford, P. C.; Sanbonmatsu, K. Y.; Onuchic, J. N. SMOG@ctbp: Simplified Deployment of Structure-Based Models in GROMACS Nucleic Acids Res. 2010, 38 (SUPPL. 2) W657 10.1093/nar/gkq498
29. Terakawa, T.; Takada, S. Multiscale Ensemble Modeling of Intrinsically Disordered Proteins: P53 N-Terminal Domain Biophys. J. 2011, 101 (6) 1450-1458 10.1016/j.bpj.2011.08.003
30. Li, W.; Wolynes, P. G.; Takada, S. Frustration, Specific Sequence Dependence, and Nonlinearity in Large-Amplitude Fluctuations of Allosteric Proteins Proc. Natl. Acad. Sci. U. S. A. 2011, 108 (9) 3504-3509 10.1073/pnas.1018983108
31. Chu, J.-W.; Izveko, S.; Voth, G. A. The Multiscale Challenge for Biomolecular Systems: Coarse-Grained Modeling Mol. Simul. 2006, 32, 211-218 10.1080/08927020600612221
32. Li, W.; Terakawa, T.; Wang, W.; Takada, S. Energy Landscape and Multiroute Folding of Topologically Complex Proteins Adenylate Kinase and 2ouf-Knot Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (44) 17789-17794 10.1073/pnas.1201807109
33. Li, W.; Wang, W.; Takada, S. Energy Landscape Views for Interplays among Folding, Binding, and Allostery of Calmodulin Domains Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 10550-10555 10.1073/pnas.1402768111
34. Hori, N.; Takada, S. Coarse-Grained Structure-Based Model for RNA-Protein Complexes Developed by Fluctuation Matching J. Chem. Theory Comput. 2012, 8 (9) 3384-3394 10.1021/ct300361j
35. Knotts, T. A.; Rathore, N.; Schwartz, D. C.; de Pablo, J. J. A Coarse Grain Model for DNA J. Chem. Phys. 2007, 126 (8) 084901 10.1063/1.2431804
36. Sambriski, E. J.; Schwartz, D. C.; De Pablo, J. J. A Mesoscale Model of DNA and Its Renaturation Biophys. J. 2009, 96 (5) 1675-1690 10.1016/j.bpj.2008.09.061
37. Hinckley, D. M.; Freeman, G. S.; Whitmer, J. K.; De Pablo, J. J. An Experimentally-Informed Coarse-Grained 3-Site-per-Nucleotide Model of DNA: Structure, Thermodynamics, and Dynamics of Hybridization J. Chem. Phys. 2013, 139 (14) 144903 10.1063/1.4822042
38. Freeman, G. S.; Hinckley, D. M.; Lequieu, J. P.; Whitmer, J. K.; de Pablo, J. J. Coarse-Grained Modeling of DNA Curvature J. Chem. Phys. 2014, 141 (16) 165103 10.1063/1.4897649
39. Lu, X. J.; Olson, W. K. 3DNA: A Software Package for the Analysis, Rebuilding and Visualization of Three-Dimensional Nucleic Acid Structures Nucleic Acids Res. 2003, 31 (17) 5108-5121 10.1093/nar/gkg680
40. Jackson, M. B. Molecular and Cellular Biophysics; Cambridge University Press: Cambridge, U.K., 2006.
41. Stormo, G. D. Introduction to Protein-DNA Interactions: Structure, Thermodynamics, and Bioinformatics; Cold Spring Harbor Laboratory Press: New York, 2013.
42. Terakawa, T.; Takada, S. RESPAC: Method to Determine Partial Charges in Coarse-Grained Protein Model and Its Application to DNA-Binding Proteins J. Chem. Theory Comput. 2014, 10 (2) 711-721 10.1021/ct4007162
43. Ono, J.; Takada, S.; Saito, S. Couplings between Hierarchical Conformational Dynamics from Multi-Time Correlation Functions and Two-Dimensional Lifetime Spectra: Application to Adenylate Kinase J. Chem. Phys. 2015, 142, 212404 10.1063/1.4914328
44. Kanada, R.; Kuwata, T.; Kenzaki, H.; Takada, S. Structure-Based Molecular Simulations Reveal the Enhancement of Biased Brownian Motions in Single-Headed Kinesin PLoS Comput. Biol. 2013, 9 (2) e1002907 10.1371/journal.pcbi.1002907
45. Luijsterburg, M. S.; Noom, M. C.; Wuite, G. J. L.; Dame, R. T. The Architectural Role of Nucleoid-Associated Proteins in the Organization of Bacterial Chromatin: A Molecular Perspective J. Struct. Biol. 2006, 156 (2) 262-272 10.1016/j.jsb.2006.05.006
46. Murphy, F. V.; Churchill, M. E. Nonsequence-Specific DNA Recognition: A Structural Perspective Structure 2000, 8 (4) 83-89 10.1016/S0969-2126(00)00126-X
47. Marcovitz, A.; Levy, Y. Frustration in Protein-DNA Binding Influences Conformational Switching and Target Search Kinetics Proc. Natl. Acad. Sci. U. S. A. 2011, 108 (44) 17957-17962 10.1073/pnas.1109594108
48. Terakawa, T.; Kenzaki, H.; Takada, S. P53 Searches on DNA by Rotation-Uncoupled Sliding at C-Terminal Tails and Restricted Hopping of Core Domains J. Am. Chem. Soc. 2012, 134 (35) 14555-14562 10.1021/ja305369u
49. Agback, P.; Baumann, H.; Knapp, S.; Ladenstein, R.; Härd, T. Architecture of Nonspecific Protein-DNA Interactions in the Sso7d-DNA Complex Nat. Struct. Biol. 1998, 5 (7) 579-584 10.1038/836
50. Khazanov, N.; Levy, Y. Sliding of p53 along DNA Can Be Modulated by Its Oligomeric State and by Cross-Talks between Its Constituent Domains J. Mol. Biol. 2011, 408, 335-355 10.1016/j.jmb.2011.01.059
51. Levy, Y.; Onuchic, J. N.; Wolynes, P. G. Fly-Casting in Protein-DNA Binding: Frustration between Protein Folding and Electrostatics Facilitates Target Recognition J. Am. Chem. Soc. 2007, 129 (4) 738-739 10.1021/ja065531n
52. Kenzaki, H.; Takada, S. Partial Unwrapping and Histone Tail Dynamics in Nucleosome Revealed by Coarse-Grained Molecular Simulations PLoS Comput. Biol. 2015, 11 (8) e1004443 10.1371/journal.pcbi.1004443
53. Savelyev, A.; Papoian, G. A. Chemically Accurate Coarse Graining of Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 20340-20345 10.1073/pnas.1001163107
54. Freeman, G. S.; Hinckley, D. M.; Pablo, J. J. De; Freeman, G. S.; Hinckley, D. M.; Pablo, J. J. De A Coarse-Grain Three-Site-per-Nucleotide Model for DNA with Explicit Ions J. Chem. Phys. 2012, 135, 165104 10.1063/1.3652956
55. Fan, Y.; Korolev, N.; Lyubartsev, A. P.; Nordenskiöld, L. An Advanced Coarse-Grained Nucleosome Core Particle Model for Computer Simulations of Nucleosome-Nucleosome Interactions under Varying Ionic Conditions PLoS One 2013, 8 (2) e54228 10.1371/journal.pone.0054228
56. Fraternali, F.; Cavallo, L. Parameter Optimized Surfaces (POPS): Analysis of Key Interactions and Conformational Changes in the Ribosome Nucleic Acids Res. 2002, 30 (13) 2950-2960 10.1093/nar/gkf373
57. Berger, M. F.; Philippakis, A. A.; Qureshi, A. M.; He, F. S.; Estep, P. W.; Bulyk, M. L. Compact, Universal DNA Microarrays to Comprehensively Determine Transcription-Factor Binding Site Specificities Nat. Biotechnol. 2006, 24 (11) 1429-1435 10.1038/nbt1246
58. Zhao, Y.; Granas, D.; Stormo, G. D. Inferring Binding Energies from Selected Binding Sites PLoS Comput. Biol. 2009, 5 (12) e1000590 10.1371/journal.pcbi.1000590